Edible Insects Processing: Traditional and Innovative Technologies Guiomar Melgar-Lalanne , Alan-Javier Hernandez-´ Alvarez´ , and Alejandro Salinas-Castro

Abstract: Insects are part of the human diet in many parts of the world. Their nutritional value is widely recognized. Currently, most edible insects are harvested from the wild, although semi-domestication and indoor farming have increased insect availability and the sustainability of production. In traditional cultures, insects are processed in a number of ways (steaming, roasting, smoking, frying, stewing, and curing, among others) to improve their sensory and nutritional qualities as well as their shelf-life. In order to increase consumer interest in the West, various technologies have been developed that are aimed primarily at using insects as ingredients in a non-recognizable form, such as powders or flour. These technologies include drying (sun-drying, freeze-drying, oven-drying, fluidized bed drying, and microwave-drying) and new processing methods (ultrasound-assisted extraction, cold atmospheric pressure plasma, and dry fractionation) designed mainly for protein, fat, and/or chitin extraction. Insect-based ingredients are sold for the production of cookies, chocolates, tortilla-style chips, and other snacks. This review focuses on edible insect production, processing technologies, and commercialization using strategies ranging from traditional to novel as a sustainable approach for improving food security worldwide. Keywords: cooking, edible insects, food processing technologies, insect farming, neophobia, review

Introduction concerns are based on a wide variety of studies that have been Nearly 2.5 billion people in the world currently supplement conducted on the prevention of food-borne diseases (microbio- their diet with insects (Van Huis, 2016). Edible insects are mostly logical, allergenic, and chemical; van der Fels-Klerx, Camenzuli, consumed in tropical regions, which have high levels of biodi- Belluco, Meijer, & Ricci, 2018). The lack of hygiene and inad- versity, suggesting that ecological factors related to the abundance equate processing and storage conditions are viewed as a more of insect species have influenced consumption patterns (Lesnik, significant concern than the quality of the insects themselves, as 2017). In most parts of Europe, and among non-aboriginal Amer- they are not usually toxic to humans. It is crucial to implement ap- icans, Canadians, Australians, and New Zealanders, entomophagy propriate post-harvesting technologies for the conservation, trans- remains rare or even a taboo (Shelomi, 2015). Whereas in the formation, distribution, and storage of edible insects, in order to Western World, people tend to associate insects with plagues and provide products that are safe and wholesome, thereby reducing health risks, in tropical countries, they are part of culinary tradi- consumers’ fears. tions, mostly in rural areas. People in many parts of Asia, Africa, Edible insects are considered the main solution to the problem and Latin America consume whole insects in a perfectly recogniz- of how to meet the growing global demand for animal protein able form, either as snacks or as part of their daily diet. Insects are that is sought after for its high nutritional value (Bruinsma, 2003). usually boiled and dried, toasted, or fried before being incorpo- Although edible insects generally have a high nutritional value, rated into different dishes. nutrient composition varies with the species, life stage, sex, and Despite the high nutritional quality of edible insects, concerns diet. The nutritional value of edible insects is widely recognized have been raised about the lack of sanitary and quality controls (Ayensu, Annan, Edusei, & Lutterodt, 2019; Elhassan et al., 2019; applied in connection with their sale. Insects are typically sold in Feng et al., 2017; Rumpold & Schluter,¨ 2013). In Figure 1, a bulk, a situation that has worried public health officials with re- short summary of the nutritional content of the nine insect orders sponsibility for food safety (Belluco et al., 2013; UN, 2015). Such is provided. Most of the species analyzed belonged to the order Orthoptera (grasshoppers, locusts, and crickets) and Lepidoptera (caterpillar). The least represented orders were Odonata (drag- CRF3-2019-0016 Submitted 1/17/2019, Accepted 5/15/2019. Author Melgar- Lalane is with Inst. de Ciencias Basicas,´ Univ. Veracruzana, Av. Dr. Luis Caste- onflies) and Blattodea (cockroaches). Insects are rich in protein lazo Ayala s/n. Col Industrial Animas,´ 91192, Xalapa, Veracruz, Mexico. Author (35.34 g/100 g dry weight (dw) for termites to 61.32 g/100 g dw Hernandez-´ Alvarez´ is with School of Food Science & Nutrition, Univ. of Leeds, LS2 for grasshoppers) and lipids (13.41 g/100 g dw for grasshoppers 9JT, Leeds, UK. Author Salinas-Castro is with Direccion´ General de Investigaciones, to 33.40 g/100 g dw for beetles). The lipid fraction is of high Av. Dr. Luis Castelazo Ayala s/n. Col Industrial Animas,´ 91192, Xalapa, Veracruz, quality, being rich in mono- and polyunsaturated fatty acids, with Mexico. Direct inquires to author Melgar-Lalanne (E-mail: [email protected]). a high omega 3: omega 6 (ω´ -3/ω´ -6) ratio (Zielinska,´ Baraniak,

C 2019 Institute of Food Technologists® r doi: 10.1111/1541-4337.12463 Vol. 00, 2019 Comprehensive Reviews in Food Science and Food Safety 1 Edible insects processing . . .

Figure 1–Nutritional composition of edible insect orders (1 g/100 g dry matter (adapted from Rumpold & Schluter,¨ 2013). NFE, nitrogen-free extract; number of species considered by order: Blattodea: 3, Coleoptera: 45, Diptera:6,Hemiptera: 27, Hymenoptera: 45, Isoptera:7,Lepidoptera: 50, Odonata:2,Orthoptera: 51.

Kara´s, Rybczynska,´ & Jakubczyk, 2015). Insects also have a high perfectly recognizable forms (Sogari, Menozzi, & Mora, 2019; chitin content, which ranges from 11.6 to 137.2 mg/kg in com- Verbeke, 2015), while young adults, especially those with higher mercially raised insects (Finke, 2007). Given their low methane levels of education, are the most likely to be willing to try insect- production, insects can play a key role in the fight against global based foods (Hartmann, Shi, Giusto, & Siegrist, 2015). Although warming (Van Huis & Dunkel, 2017). Unless food policies and changes in food choices are difficult to predict, a number of other eating habits change, the global food crisis could reach unprece- new foods have achieved acceptance over the years, such as sushi, dented levels with consequent risks to worldwide food security quinoa, and kale. Other recent introductions to the market include (Spiegel, Noordam, & van der Fels-Klerx, 2013). However, as kefir, kombucha tea, and goji berries, which were completely mentioned earlier, insect consumption in the West is limited by unknown to consumers in the West just a few years ago (Shelomi, the lack of industrialization strategies and by food neophobia. 2015). A number of production and storage strategies have been de- In some European countries, consumers have shown an interest veloped to improve processing technologies. There is growing in new food products that use insects as ingredients in an un- interest among entrepreneurs in semi-domestication of insects in recognizable form (Figure 2). For example, if insects are used in the wild and indoor farming (Varelas & Langton, 2017). Unfor- flours or powder, or are added to different products, such as energy tunately, to date, only a few species can be considered fully do- drinks, cookies, and corn tortillas, consumers, particularly young mesticated, including bees, silkworms, and cochineals, while ter- people, are more likely to accept them (Hartmann & Siegrist 2016; mites, flour worms, and crickets are considered semi-domesticated Hartmann & Siegrist 2018). This is a promising market niche that (Vantomme, 2015). Various technologies can be used: tradi- should be targeted through the development of food technologies tional sun-drying (Manditsera, Lakemond, Fogliano, Zvidzai, & and innovations. Luning, 2018), microwave processing (Vandeweyer, Lenaerts, Cal- Another area of interest consists of the development of lens, & Van Campenhout, 2017), freeze-drying, oven-drying functional ingredients for food, feed, pharmaceutical, and (Fombong, Van Der Borght, & Vanden Broeck, 2017), dry frac- industrial applications. Ingredients of interest such as chitin tionation (Purschke, Bruggen,¨ Scheibelberger, & Jager,¨ 2018a), (Song et al., 2018), oleic acid (Purschke, Stegmann, Schreiner, & freezing (Melis et al., 2018), marination, and fermentation (Bor- Jager,¨ 2017; Sun et al., 2018), proteins (Bußler, Rumpold, Jander, remans, Lenaerts, Crauwels, Lievens, & Van Campenhout, 2018). Rawel, & Schluter,¨ 2016; Huang et al., 2018; Ndiritu, Kinyuru, In addition, several modified atmosphere packaging methods have Kenji, & Gichuhi, 2017), and bioactive peptides (Montowska, been explored to increase the shelf-life of these products (Stoops Kowalczewski, Rybicka, & Fornal, 2019; Nongonierma & et al., 2017). Also, various “disguised insect products” have been FitzGerald, 2017; Zielinska,´ Kara´s, & Jakubczyk, 2017) have been successfully formulated, such as chocolates, cookies, and ground partially or totally extracted and purified. Nonetheless, scaling beef, among others (Azzollini, Derossi, Fogliano, Lakemond, & up these processes to the industrial level would still be too costly Severini, 2018; Homann, Ayieko, Konyole, & Roos, 2017; Walia, (Lamsal, Wang, Pinsirodom, & Dossey, 2019). Kapoor, & Farber, 2018). In summary, the production, processing, and storage of ed- In general, eating behavior is influenced by the social context ible insects are achieved using a variety of approaches ranging and shaped largely during early childhood (Higgs & Thomas, from conventional to innovative. Food neophobia, sustainability, 2016; Scaglioni et al., 2018). In Western countries, women are and convenience have a significant influence on the introduction more reluctant than men to eat insects, particularly in whole and of insect products to the market (Dobermann, Swift, & Field,

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Figure 2–Some edible insect food preparations (courtesy of Chef Mario Melgarejo Pin˜on´ ).

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2017). This review focuses on edible insect production and pro- experience with Australian Aborigines. In Kenya, the Interna- cessing technologies, and commercialization using strategies rang- tional Centre of Insect Physiology and Ecology is a pioneer in ing from traditional to novel as a sustainable solution for food implementing “ecotourism mechanisms” involving the sustain- security worldwide. able use of natural forest products, including commercial insects. However, the long-term impact of these experiences has not been Food Neophobia and Aversion to Insect Consumption sufficiently explored (Yen, Hanboonsong, & Van Huis, 2012). The development of taste starts in utero and it is shaped, at the Tourism, recommendations from close relatives or friends, and most basic level, by biological factors, including an innate pref- increasing media attention may encourage insect consumption, erence for sweet foods and an innate aversion to bitter and sour mostly by early-adopters (Sogari, Menozzi, & Mora, 2017; Van flavors (Ventura & Worobey, 2013). These preferences can change Thielen et al., 2018). Culinary tourism could help introduce peo- over time with repeated exposure and pragmatic learning through ple to new foods, since tourists are usually more motivated to complex social, cultural, and even religious systems, depending change their habits and willing to try something unusual dur- on factors such as age, gender, health status, education, and in- ing their vacations (Dimitrovski & Crespi-Vallbona, 2017). When come level (Giordano, Clodoveo, De Gennaro, & Corbo, 2018). tourists return home, they may have a positive influence on people Although food taste preferences are related to the flavor of foods, close to them by increasing familiarity and allaying concerns (Bar- they are also viewed as the set of preferences and/or aversions as- sics et al., 2017). In regions with a long history of entomophagy, sociated with emotional and cultural states (Wright, Nancarrow, many food festivals are held, targeting domestic tourists; therefore, & Kwok, 2001). Food taste preferences reflect a spectrum of at- consumption is related with many different factors as tradition, titudes, from neophobia, fear of tasting new food, to neophilia, identity and nostalgia (Sun-Waterhouse et al., 2016). In Thailand, just as curiosity about and the desire to try novel food sources. the number of visitors to cricket farms, ethnic restaurants, and tra- Neophobia is strongly associated with fear of the unknown for ditional markets has risen in recent years (Halloran, Roos, Flore, & sanitary, cultural, or even religious reasons (Giordano et al., 2018; Hanboonsong, 2016). Interest in eating insects is also increasing Hartmann & Siegrist, 2018), and neophilia is associated with the in countries without this legacy. For example, the North Carolina development of cuisine, which allows the incorporation of new Museum of Natural Sciences holds an annual “Bug-Fest,” which is food items into the diet to satisfy the need for variety (Armelagos, attended by more than 35,000 people who “taste delectable dishes 2014). featuring creepy crawlers” as a major ingredient at “Cafe´ Insecta” Neophobia is closely related to the emotion of disgust. Disgust, (Perdue, 2018). In summary, culinary tourism is a useful avenue for a primary emotion related to sensory qualities, such as appear- exploring the multiple dimensions of entomophagy. Eating insects ance, taste, and aroma, is determined by the implicit association can be considered a novel strategy with positive ethical implica- that people have with the disgust-eliciting object. Disgust is more tions for addressing global warming but also, is an important way difficult to eliminate than neophobia. However, both neophobia to recognize the tradition and culture in many parts of the world and disgust contribute to individuals’ unwillingness to include a (Perdue, 2018). specific food in their daily diet (La Barbera, Verneau, Amato, & Gender, age, health status, and income are other important Grunert, 2018). Judging from the findings of blindfolded sensory factors that affect preferences with respect to trying edible insects. taste experiments in which participants had difficulty identifying Gender influences preferences related to the visual appearance of edible insect products (Meyer-Rochow & Hakko, 2018), sight insect-based products, with women being more traditional in their may have a more significant influence on disgust toward insects. choices than men, and therefore more reluctant to try these types The positive attitude needed to overcome food neophobia im- of products (Caparros Megido et al., 2016). Younger males show plies an interest in novel foods and enjoyment of a wide vari- a more open attitude than women to including insects in their ety of foods, even unfamiliar ones. This positive attitude may diets as a meat substitute in keeping with their concerns about the be related to the strength and characteristics of each food culture. environmental impact of their food choices (Verbeke, 2015). Some studies blame culinary maturity in Western cultures for their In order for insect-based foods to be adopted in the West, they negative attitude toward consuming insects (Piha, Pohjanheimo, must taste good, be attractive to consumers, and be readily avail- Lahteenm¨ aki-Uutela,¨ Kˇreckovˇ a,´ & Otterbring, 2018). However, able (Hartmann & Siegrist, 2016; Tan, Verbaan, & Stieger, 2017). this point is not clear enough. Willingness to try novel foods has Strategies like ethnic food markets and festivals have been devel- been found to vary from country to country. Swedes are more oped to allow early-adopters to try whole, recognizable insects. willing to do so than Americans and Finns, and Koreans are more Other strategies consist of promoting insects as an alternative to reluctant than Americans (Dimitrovski & Crespi-Vallbona, 2017). nuts and chips, since these snack foods have similar characteris- Some studies have shown that North Americans and Europeans tics such as texture, macronutrient content, and flavor (Shelomi, are willing to eat insects if they are in an unrecognizable form. 2015). Therefore, processing methods may promote consumption in the Approaches for using edible insects in familiar foods (e.g., in- future. In practice, dried insects may be crushed or pulverized, corporation into burgers, cookies, or chips) as a transitional phase and raw or boiled insects can be ground or mashed, making them in which minced or powdered insects are incorporated into com- unrecognizable (Menozzi, Sogari, Veneziani, Simoni, & Mora, mon ready-to-eat preparations in small amounts have also been 2017; Mlcek, Borlovcova, Rop, & Bednarova, 2018). tried (Van Thielen et al., 2018). Processed foods, such as cookies There are many ways in which insects are associated with recre- or chips, containing only a small amount of insect flour are better ational activities and tourism and become part of culinary expe- accepted by consumers and allow them to become familiar with riences (Perdue, 2018). The tourism experience involves eating edible insects (Caparros Megido et al., 2017; Hartmann & Siegrist, insects as part of “ecotourism vacations,” with the ultimate aim 2016). Nevertheless, the use of familiar preparations has not always of maintaining the biodiversity of native ecosystems. This is the led to the acceptability of the final prepared product because con- case for tourism excursions to the headwaters of the Amazon in sumers usually expect the insect preparations to have a taste that is Ecuador, Ariau in Brazil, Tado in Indonesia, and the bush-tucker inferior to that of the original products, even if they are visually

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Table 1–Number of edible insect species consumed, in order of importance and by biogeographical region (adapted from Jongema, 2017).

Order Common name Afr. Au. Neartic Neotrop. Or. Pal. Araneae Spiders 4 2 0 4 8 0 Coleoptera Beetles 89 29 18 215 282 84 Dermaptera Earwigs 0 0 0 0 1 Dictyoptera Cockroaches, termites and mantids 4 3 0 6 18 12 Diptera Flies 5 1 15 12 3 6 Ephemeroptera Mayflies 2 2 0 2 3 3 Hemitera heteroptera True bugs 17 4 0 46 54 14 Hemitera homoptera Cicadas 27 12 12 20 30 26 Hymenoptera Ants, Bees, Wasps and Sawflies 32 14 23 224 42 51 Isoptera Termites 34 1 1 18 17 16 Ixodida Ticks 1 0 0 0 0 0 Lepdidoptera Butterflies and moths 146 28 11 108 23 93 Megaloptera Alderflies, Fishflies, Dobsonflies 0 0 0 2 0 2 Odonata Dragonflies 3 2 1 15 34 7 Orthoptera Grasshoppers 107 7 14 72 95 33 Phasmida Ghost insects 0 2 0 1 4 0 Plecoptera Stoneflies 0 0 2 0 2 5 Phthiraptera Lice 0 0 0 3 1 0 Psocoptera Bark flies 0 0 0 1 0 0 Trichoptera Caddisflies 0 0 0 5 1 4 Total of species 471 107 97 754 618 356

Biogeographical regions: Afr.: Tropical Africa, Au: Australia; Neotrop.: Neotropics; Or.: Orient.; Nearctic: Nearctic; Pal: Palearctic. identical. Preconceptions about the taste of a food tend to be more shame and as being related to poverty and a provincial mindset. negative when the individual has never tasted the food before (Tan This contradiction is evident in countries like Mexico where insect et al., 2017; Woolf, Zhu, Emory, Zhao, & Liu, 2019). Perceptions markets, restaurants, and ethnic festivals have become increasingly differ between novel and common foods, and the development popular among high- and middle-class tourist populations in urban of new products requires the selection of the appropriate type of areas, while consumption, harvesting, and farming are declining in products and adjustment of their properties to match consumer rural areas associated with poverty. Despite the growing demand motivations compared with taste expectations (Tan et al., 2017). for edible insects in urban areas, production through wild harvest- Good product development is crucial, and includes making the ing and indoor farming is still limited, because farmers associate products more attractive to consumers and encouraging repeated insects with poverty and do not view it as a potential source of consumption through incentives (Hartmann & Siegrist, 2016; Tan income (Ramos-Elourdy, Pino-Moreno, & Mart´ınez-Camacho, et al., 2017). 2012). Even when insects are consumed as “invisible” ingredients, con- To increase the inclusion of insects in daily diets, a successful sumers must have a reason to choose the insect-based product so strategy to consider involves serving snacks between meals. These that they will consume it on a regular basis. Reasons for such types of snacks are increasing in popularity in the global market choices relate more to factors such as visual appearance, taste, and are attractive to early adopters (Shelomi, 2015; Tan et al., good value, and availability than to environmental sustainability or 2017). protein quality (House, 2016). Market availability of the products (whole or processed) and type of communication with consumers Farming Edible Insects are primary factors in increasing the acceptance and consumption The growing demand for edible insects has created a challenge, of insects in Western countries (Sogari et al., 2017). However, in- namely the production of more edible insects in an economically troducing insect products may require promotional efforts that go efficient, safe, and sustainable manner (Gahukar, 2011). The lack beyond messages related to the positive environmental impact and of availability creates accessibility issues, and therefore, reduces op- nutritional value of edible insects. This could include official and portunities for increasing trade (Shelomi, 2015). These two factors mass media recommendations aimed at facilitating the interaction point up the need to make the technological leap from wild har- between consumers and insect foodstuffs (Alemu, Olsen, Vedel, vesting to indoor farming. In this sense, traditional indigenous Pambo, & Owino, 2017). Other strategies, such as food festivals knowledge associated with wild harvesting and local insect con- and ethnic festivals, could promote entomophagy by reducing the sumption can complement the scientific knowledge required to attendees’ fear of tasting these types of products (Aguanta, 2018; boost the supply of insects through large-scale farming (Raheem Barsics et al., 2017). et al., 2018). Traditional consumer countries are grappling with their own Harvesting from the wild (forests, waterways, or agricultural complex neophobia issues owing to the fact that neophagia is as- fields) is the most traditional way to gather insects. A large vari- sociated with a perception of poverty. The problem is even more ety of species at various life stages can be collected, in keeping pronounced in urban areas, and some African countries, includ- with the traditional and cultural practices of small-scale producers ing Zimbabwe, Nigeria, and Botswana, have reported that young (Van Huis & Oonincx, 2017). These producers have the nec- people are rejecting entomophagy (Ebenebe & Okpoko, 2015; essary expertise to recognize the proper timing, conditions, and Manditsera et al., 2018; Obopile & Seeletso, 2013). Although, in host vegetation in order to produce specific edible species with- the West, edible insects are being promoted as an environmen- out damaging the environment (Durst & Hanboonsong, 2015). tally sustainable protein source to young people in higher income Insects are collected from fields mainly for home consumption, a brackets, young people in countries where entomophagy is a tra- practice that has a low environmental impact and helps maintain ditional practice still perceive insect consumption as a source of insect resources at a fairly constant level over time. Traditional

r C 2019 Institute of Food Technologists® Vol. 00, 2019 Comprehensive Reviews in Food Science and Food Safety 5 Edible insects processing . . . harvesting has been carried out in Mexico since pre-Hispanic people in some areas of Thailand collect young wasp nests and times when insects were not considered pests, but rather an im- protect them until they are ready to eat. Bamboo caterpillars are portant food source (Cerritos & Klewer, 2015), and more than generally packed in plastic boxes and sold in local markets (Durst 400 insect species were harvested from the wild (Cerritos & Cano- & Hanboonsong, 2015). In Africa and Asia, semi-domesticated Santana, 2008), mostly from terrestrial ecosystems. The harvesting bees are reared in wooden hives, old tree trunks, or other contain- of each species is unique and depends on the stage of development ers (DeFoliart, 1997). Similarly, in Manchuria (China), silkworms (eggs, pupae, larvae, or adults), season (rain or dry), and loca- have been semi-domesticated to produce silk as well as food and tion (forest, desert, or agricultural fields). Pupae of the ant species feed with optimal stocking, to prune trees to control crown de- Limetopum apicuatum (escamoles) are collected during the warm dry velopment and promote leaf flushing, and to produce fertilizer season (February to May) and the eggs are removed from the for legumes (Xiang et al., 2010). Weaver ants construct nests by anthills (Lara-Juarez,´ Rivera, Lara, & Reyes-Aguero,¨ 2018); red weaving leaves together using larval silk. Some farmers in Thailand maguey worms (Hypopta agavis) are picked from the pineapples maintain colonies in host trees; the ants are harvested once a year of the maguey (Agave saliminara) after the start of the rainy sea- (Hanboonsong, Jamjanya, & Durst, 2013) and used for medicinal son (Juarez-Ortega,´ Viesca-Gonzalez,´ & Barrera-Garc´ıa, 2012); and culinary purposes. and grasshoppers belonging to the species Sphenarium purpuras- Domestication of edible insects is relatively simple and econom- cens (chapulines) are manually harvested from fields when the rainy ical, although nowadays only three species are considered fully do- season starts (Cerritos & Cano-Santana, 2008). mesticated: bees, silkworms, and cochineals; several other species Agricultural intensification poses a threat to many edible in- are partly domesticated. The main reasons for this are: (1) most in- sects, primarily as a result of mechanization, tree clearance, and sects can be easily reared in small spaces or containers; (2) their life pesticide use. Pesticides have caused a decline in insect populations cycle is short; (3) they can eat forest or agricultural wastes instead worldwide, with a 67% decline in invertebrate populations in the of grains; (4) insect farming can be carried out in both urban and last 40 years (Payne & Van Itterbeeck, 2017). If agrochemical con- rural areas; and (5) short-term financial returns are possible. House trols were eliminated, the potential yield of a specific grasshopper crickets and yellow mealworms are the most widely farmed in- species in Mexico would generate an estimated annual income sects in the world due to their commercial success; however, they of nearly US$350,000 and would provide enough protein to feed are mostly sold as pet food (Gahukar, 2016). Most farmed insects close to 9 million people annually (Cerritos-Flores, Ponce-Reyes, can be easily raised in small ventilated plastic containers at high & Rojas-Garc´ıa, 2014). ambient temperatures (up to 30 °C) and relative humidity (up Uncontrolled overharvesting is causing ecological damage due to 70%) and are fed organic wastes and cereals. They have low to changes in the trophic chain (Gahukar, 2016; Van Huis & technical requirements, high production densities, and do not re- Oonincx, 2017). The increased demand for a few insect species quire sunlight during some life stages (Hanboonsong et al., 2013). has led to more aggressive harvesting techniques, without appro- The most commonly farmed insect is T. molitor L. In a recent priate care being exercised to ensure sustainable collection during review, Soares-Araujo,´ dos Santos Benfica, Ferraz, and Moreira reproductive periods—a practice that could reduce or even elimi- Santos (2019) concluded that the optimal rearing temperature was nate local biodiversity (Durst & Hanboonsong, 2015; Van Huis & 25 to 28 °C with relative humidity close to 70%, and the diet Oonincx, 2017). For example, the overexploitation of honey ants must contain 5% to 10% yeast, 80% to 85% carbohydrates, and B and wood grubs in Australia linked to demand from restaurants complex. There are many different strategies for feeding insects, and ecotourism threatens their availability (Yen, 2009). Similarly, including the use of food by-products and organic wastes. How- in the state of Hidalgo, Mexico, 18 edible insect species have been ever, a diet with high protein (around 20%) and high fat (around reported to be at risk of extinction due to overharvesting, habitat 9%) contents is required to obtain the best results in terms of feed changes and pollution (Ramos-Elourdy, 2006). The development conversion efficiency, survival, development time, and nutritional of sustainable techniques could reduce or even avoid the use of composition. Bran or other by-products can be used as comple- pesticides in agriculture that would have a positive impact on ments in the diet (Oonincx, van Broekhoven, van Huis, & van the environment (Cerritos & Cano-Santana, 2008; Van Huis & Loon, 2015). Vegetables and fruits in the diet are considered only Oonincx, 2017). The long-term damage that overharvesting as a water source, and a small quantity of water is added to pre- causes to the environment and native insect populations is still un- vent fungal contamination (Oonincx et al., 2015; Ramos-Elourdy, known. Efforts should be focused on prohibiting harvesting during 2006; Soares-Araujo´ et al., 2019). breeding periods and using less destructive harvesting techniques In Thailand, cricket farming was introduced in 1997, and crick- (Durst & Hanboonsong, 2015). ets are currently sold directly to consumers and to other farmers The environmental and health risks have prompted an increase at local and urban markets. Some producers are grouped in coop- in the semi-domestication of some edible wild insect species eratives and are recognized as important contributors to the rural in a more sustainable, less time consuming, and more consis- economy and employment. Species preferred by consumers have tent manner, mostly in traditional consumer countries where the been selected for indoor farming (Halloran et al., 2016). warm, wet weather is appropriate for farming (Varelas & Langton, 2017). Semi-domesticated populations are those whose morpho- Traditional Cooking logical, behavioral, physiological, and/or life-history traits result Studies have shown that traditional insect consumption is higher from human management actions, which involve partial control at lower latitudes, that is, in tropical regions of the world (see over breeding, mortality, space use, and food supply designed to Table 1). Around the world, insects are consumed in 11 Euro- increase potential economic profit (Mysterud, 2010). Outdoor pean countries, 14 countries in Oceania, 23 American countries, farming includes rearing insects in old trees, sawdust, and forest 29 Asian countries, and 35 African countries. Mexico, China, wastes that, in addition to providing a semi-confined habitat, can Thailand, and India are the leading consumer countries in the be a source of food. In Thailand, bamboo caterpillars mate in world and those with the most species described as Table 1 shows nylon net cages placed over growing bamboo shoots. In addition, (Jongema, 2017).

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Table 2–Blanching treatments usually applied to edible insects.

Insect species Blanching treatment Main findings Reference Alphitobius Submerged in bath with water at Reduction in total microbial count Wynants et al., 2018 diaperinus (beetle) 90 °C until water temperature of 4.0 log cfu/g but aerobic reaches 88 °C(5min). endospores persisted. No typical pathogens were identified. Some mold producers of mycotoxins found. Ruspolia differens Submerged in boiling water for Not indicated. Fombong et al., 2017 (grasshopper) 5 min, drained, and allowed to cool. Tenebrio molitor L. Submerged for 10 min in boiling Slight increase in water content Purchke et al., 2017 (mealworm larvae) water in a 1/12 (w/w) but no significant changes in larvae-water ratio. composition of macronutrients. Tenebrio molitor L. Submerged for 1 min in boiling Reduction in TVC (with boiling Caparros Megido (live larvae) water or sterilized in cans with 4 log cfu/g) and sterilization et al., 2017 brine solution (5% NaCl) for (5 log cfu/g); No yeast or mold 16 min at 120 °C. observed with either treatment. Archea domesticus Submerged in boiling water for Reduction in TVC with boiling Caparros Megido (house cricket) 4 min or sterilized in cans with (4 log cfu/g) and sterilization et al., 2017 brine solution (NaCl 5%) for (5 log cfu/g); No yeast or mold 16 min at 120 °C. observed with either treatment. Macrotermes spp. Submerged in boiling water for Reduction in TVC (3 log cfu/g) Caparros Megido (smoked termites) 1min. with boiling. No yeast or mold et al., 2017 observed with either treatment. Cirina gorda Submerged in boiling water for Reduction in TVC (3 log cfu/g). Caparros Megido (mickwater 5min. No yeast or mold observed with et al., 2017 caterpillar) either treatment. Tenebrio molitor L. Submerged in boiling water for Increase in water content. Azzollini et al., 2016 (mealworm) 3 min in a 1/10 (w/w) No significant changes in larvae-water ratio. composition of macronutrients. Drained for 2 min, and excess Decrease in luminosity color water removed with absorbent factor. paper. No microbiological data. Tenebrio molitor a) Submerged in boiled water: No significant differences in TVC, Klunder et al., 2012 (mealworm larvae) -1min Ent, or BS were found with -10min different boiling treatments. - 5 min followed by With roasting, more Ent were oven-drying at 55 °C, detected both in whole and 24 hr crushed forms. - 1mininacidwater(pH 4.0) b) Roasting for 10 min whole and crushed.

Archeta domesticus a) Submerged in boiling water Better TVC results were found by Klunder et al., 2012 (cricket) for 5 min. submerging in boiling water; b) Stir-frying for 5 min. No differences in Ent and BS.

Brachytrupus sp. Submerged in boiling water for 5 No differences were found in TVC, Klunder et al., 2012 (large cricket) or 10 min. Ent, or BS. Tenebrio molitor L. Submerged in boiling water in a TVC was reduced by between 5 to Vandeweyer et al., (mealworm larvae) 1/10 larvae/water ratio (w/v) 6 log cfu/g, 2017 for 10, 20, or 40 s, followed by Enterobacteriaceae, BAL, and chilling in an ice bath for 30 s. yeasts and molds almost disappeared. BS were maintained. Longer treatments were more effective. Archeta domesticus L. Submerged in boiling water Not determined. Kamau et al., 2018 (house crickets) (98 °C) for 5 min. Hermetica ilucens L. Submerged in boiling water Not determined. Kamau et al., 2018 (Black soldier fly) (98 °C) for 5 min. Where TVC, total viable count; Ent, Enterobacteriaceae; BS, bacterial spores; and LAB, Lactic acid bacteria.

The high biodiversity and relative abundance of species play a cooking procedures can increase the shelf-life of food products by key role in determining patterns of consumption, more so than reducing foodborne and degradative enzymes. From a nutritional agriculture and farming factors (Lesnik, 2017). It is estimated that perspective, cooking enhances the digestibility and bioactivity of more than 3,000 ethnic groups around the world consume insects proteins in the digestive tract; however, some nutrients could be in many forms, including hunter-gatherers (Ramos-Elourdy et al., lost through solubilization, leakage, inter- and intra-biochemical 2012; Van Huis, 2016). reactions, or new by- product (Caparros Megido et al., 2018). Heat Cooking improves sensory quality through the formation of aro- treatment may induce proteolysis, lipid oxidation, and solubiliza- matic compounds as well as changes in color and texture. Some tion of vitamins and minerals (Juarez-Ortega´ et al., 2012). Protein

r C 2019 Institute of Food Technologists® Vol. 00, 2019 Comprehensive Reviews in Food Science and Food Safety 7 Edible insects processing . . . denaturation, amino acid destruction or modification, and Mail- 11 orders have been identified as edible, only 10 to 20 species are lard reactions may also occur. Lipids and fatty acids may be auto- regularly used as food or medicine (Feng et al., 2017). The most oxidized, thermo-oxidized, or photo-oxidized (Frankel, 2012). popular insects are grasshoppers, silkworm pupae, wasps, bam- There are several traditional edible insect cooking techniques, boo insects, and stink bugs. Insects are usually fried (deep-fried including steaming, roasting, smoking, frying, stewing, and curing or quick-fried), braised, stewed, boiled, steamed, or roasted. Al- (see Figure 2; Ebenebe et al., 2015; Graboswski & Klein, 2017; though the use of insects is traditional, these are also considered Lautenshlager¨ et al., 2016; Nonaka, 2009; Obopile & Seeletso, a gourmet food in urban areas since they are perceived as “or- 2013; Ramos-Rostro et al., 2016; Shockley, Lesnik, Allen, & ganic” (free of additives, pesticides, or other artificial compounds; Munoz,˜ 2018). These techniques are preceded by blanching to Van Huis, 2016). Some insects are used in traditional medicine reduce foodborne microorganism counts and to inactivate en- for their health benefits, some of which have been scientifically zymes (Marshall, Dickson, & Nguyen, 2016). Obviously, each proven. For example, the Chinese caterpillar fungus enhances the technology generates products with different sensory qualities and immune system and has anticancer properties, and “ant alcohol” nutritional attributes (Kouˇrimska&Ad´ amkov´ a,´ 2016; Tan et al., is used to improve human sex drive (Chen, Feng, & Chen, 2009; 2017). Feng et al., 2017). In Yunnan, a type of ant is used to make vinegar In Latin America, Mexico is the country with the strongest (Feng et al., 2017). In recent years, insect menus and cookbooks tradition of eating insects. Grasshoppers and crickets (“chapulines”) have been published in South Asia to teach consumers how to cook are commonly toasted or roasted in a pan without oil until the insects. Thailand is an example of a country with an important insects are crunchy. They are collected from the start of the rainy tradition of insect consumption that is becoming more western- season in late spring until early winter. When the insects are boiled, ized (Yen, 2015). Close to 200 species of insects are consumed in the water used can be acidified with lemon juice or vinegar, and Thailand and are prepared in several innovative ways apart from the flavoring ingredients, such as garlic and onion, may be added. Af- most common (roasting, frying, and steaming), such as curried, ter toasting, when the insects are still hot, lemon, salt, and chili dipped (mixed with chili paste), and salted (Halloran, Vantomme, are usually added. During boiling, the insects turn a reddish color Hanboonsong, & Ekesi, 2015; Raheem et al., 2018). However, and aromatic compounds form. In Oaxaca, before blanching, the consumption is regional. For example, crickets are considered a insects are fasted for 1 to 3 days food to avoid the generation of specialty in northeastern Thailand, but remain rare in restaurants in bitter tastes. Many traditional dishes are made with chapulines,such Bangkok, where they are associated with rural poverty (Halloran as tacos (corn tortilla with insects and hot sauce), hot chili sauces et al., 2016). (chili sauce with chapulines), and “chiles rellenos” (chiles stuffed Entomophagy is practiced on a large scale by the tribal com- with chapulines). Chapulines are also consumed as a snack with alco- munities of northeastern India. More than 82 insect species in holic beverages (Cohen, Sanchez,´ Mata, & Montiel-Ishino, 2009; nine different orders form a major component of their main nu- Ramos-Elourdy, 1997). Similar recipes use worms as an ingre- trient intake and are reported as a normal part of the diet (Gahukar, dient, such as the maguey worm (Aegiale hesperiaris and Hypopta 2018). agavis) and yellow mealworm (Tenebrio molitor). Eggs of the ant Termites, honey bees, grasshoppers, stink bugs, aquatic insects, species Liometopum apiculatum (“escamoles”) are usually cleaned and and silkworms are cooked, roasted, pickled, or even consumed raw. then fried with either butter or oil-fried spices and eaten in taco Most of the traditional dishes are prepared by adding fresh or dried tortillas or in tamales. Other traditional culinary techniques have bamboo shoots. Crickets are mixed with salt before cooking, and been described in cookbooks (Gordon, 2013; Ramos-Elourdy & certain species like Oecophylla smaragdina (Fabr.) and Parapolybia Menzel, 1998). However, little information is available on the varia (Fabr.) are consumed raw (Mozhui, Kakati, & Changkija, safety and global quality aspects of traditional cooking practices in 2017). Mexico. Chicatana ants (Atta mexicana and Atta cephalotes), queen Africa has an impressive diversity of edible insects, with over ants collected at the beginning of the rainy season in southeast 470 species identified as edible across the continent. The highest Mexico, are prepared in chili hot sauce (Reyes-Prado, Pino- diversity is in the orders Lepidoptera, Orthoptera, and Coleoptera Moreno, Garc´ıa-Perez,´ & Carlos, 2016). (Kelemu et al., 2015). Most edible insects are harvested from the Invertebrates, which are very diverse and include many insect wild (Mutungi et al., 2017). They are cleaned (with the removal, species (more than 758 morphospecies), are traditionally used as in some cases, of certain parts, such as wings and legs), and food by at least 32 Amerindian groups (Paoletti et al., 2000). then roasted or boiled. Insects are also consumed fresh and raw. Bees, wasps, caterpillars, and beetles are the insects that are the For animal feed, insects are sun-dried and ground to a powder most commonly consumed (Paoletti et al., 2000); however, the and then added to different formulations. The edible caterpillar culinary uses of these insects have not been fully explored. Thus, Imbrasia epimethea, consumed in Angola, is collected and washed in for the Awajun, an Amazonian indigenous people of Peru, beetles water. The guts are removed to avoid aftertastes and long hairs are are the most culturally important edible insects, followed by ants, removed to avoid toxicity. The caterpillars are boiled in salty water wasps, and flies. They are prepared in a variety of ways, mostly for 30 min until the water has evaporated. They are then sun-dried roasted (67%), toasted (10%), and fried (5%) until crispy. Some for 3 days, after which they can be stored at ambient conditions. insects are eaten raw (Casas Reategui,´ Pawera, Villegas Panduro, They are fried before eating. When the thermal treatment was & Polesny, 2018). studied, no significant negative effects on nutritional value were In the Asia-Pacific region (North and Southeast Asia and Ocea- found except for a slight decrease in monounsaturated fatty nia), there is a long history of using insects as human food. In that acids (Lautenschlager¨ et al., 2017). In Tanzania, the grasshopper region, consumption of insects is tied to dietary needs, cultural Ruspolia differens is eaten fresh or processed. In both cases, various considerations, and insect availability. Insects are both harvested pretreatments are performed, such as cleaning and boiling in from the wild and farmed, and they are also used as animal feed salted water, with or without spices, for 15 min. After that, for fish and poultry (Yen, 2015). In China, the consumption of ed- the grasshoppers can be eaten, but their shelf-life is very short ible insects is widespread, and although more than 324 species from (less than 48 hr) due to high water activity (Mmari, Kinyuru,

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Laswai, & Okoth, 2017). To increase their shelf-life, insects can Table 2, blanching significantly reduces total counts of mesophilic be sun-dried for at least 2 days. Before being consumed, insects bacteria and of yeast and molds; however, it is ineffective at elim- are smoked, toasted, or fried. Smoking in a wood stove for 2 to inating, or even reducing, mesophilic bacterial spores. Blanching 4 days is common; toasting is done by placing the insects in a hot has also been reported to reduce counts of lactic acid bacteria and pan without oil until they turn brown and crunchy and acquire total psychrotrophic bacteria (Vandeweyer et al., 2017). a meat-like aroma (Fombong et al., 2017). They are also fried A slight increase in moisture has been reported after blanching, in oil for 10 min until they turn to a brownish color (Mmari (Azzollini, Derossi, & Severini, 2016; Purschke et al., 2018a). In et al., 2017). In Botswana insects are commonly consumed either T. molitor L., an increase in moisture was reported (from 62.81% without any culinary preparation or the insects are sun-dried to 70.44% after 40 s), but water activity (available water) remained before being roasted, fried, boiled, or steamed and eaten as a constant (0.96) (Vandeweyer et al., 2017). This effect could be snack. Larvae of dung beetles are grilled or fried in oil, and due to the absorption and entrapment of water inside the larva caterpillars are roasted in hot ash without salting, or salted, boiled, of T. molitor L. just below the chitinous exoskeleton. However, and sun-dried before consumption (Obopile & Seeletso, 2013). no significant differences in chemical composition between fresh In Western countries, there is no tradition of cooking insects, and blanched larvae were found (dry mass) (Azzollini et al., 2016). which significantly limits their culinary use. However, insects are Changes in chemical composition are observable at longer times, used to ferment Milbenkase¨ cheese in Germany and France; mites mostly due to leaching of soluble nutrients that can affect the are used to ferment some special varieties with a traditional lemon- protein content (Niamnuy, Devahastin, & Soponronnarit, 2008). like flavor (Bruckner¨ & Heethoff, 2016). Hence, edible insects are During the boiling process, some proteins undergo structural promoted as a snack and, like nuts, can be covered with chocolate, changes, including denaturation, crosslinking, and interaction with mixed into baked goods or sprinkled on salads. Mildly processed, lipids and carbohydrates. As a result, the number of hydrophilic fried, roasted, or finely ground, they are used to add a unique sites used for water binding may be reduced and sorption proper- flavor to foods or to increase their nutritional profile. In recent ties altered, making it necessary to conduct a more specific protein years, insect cookbooks, TV shows, food fairs, and expositions analysis (Azzollini et al., 2016). have attempted to normalize entomophagy, in contrast to previous Food color is of major importance for consumer acceptability strategies that were based on promoting the novelty of the products but it has been poorly analyzed in edible insects. Color parameters (Shelomi, 2015). However, the current high price of edible insects, have been studied in T. molitor L. flour, and luminosity (L) was compared with other sources of animal and vegetal proteins, is found to decrease with the blanching treatment, probably due to an important economic barrier to expand their market (Ramos- a physical phenomenon whereby water in fresh tissues modified Elourdy, 1997). the refraction index when compared to dry samples. Therefore, Finally, agricultural best management practices as well as good a higher moisture value in blanched samples may have altered hygiene habits need to be established and employed by edible insect the luminosity, making the samples appear darker. The solubility farmers in all countries to prevent food safety issues. Consequently, of nutrients in blanched samples may increase certain secondary standard operating procedure manuals are needed and hazard anal- reactions, such as non-enzymatic browning reactions, which can ysis and critical control points will have to be developed for raw reduce lightness (Azzollini et al., 2016). edible insects to ensure that their handling, processing, preserva- Blanching treatments should be specifically designed for each tion, storage, and packing and/or distribution until consumption insect species to improve antimicrobial effects with minimal qual- is carried out in the safest and most nutritious manner (Raheem ity loss. Blanching should minimize the microbiological risks as- et al., 2018). sociated with the consumption of edible insects, and it could be supplemented with techniques that can reduce the presence of Processing Technologies bacterial spores (Caparros Megido et al., 2017). However, to meet The edible insect industry is moving ahead at staggering speed, the requirements of consumers and industrial processing, it is es- and the demand for new products, both in recognizable form and sential for these treatments to maintain the nutritional value of the as ingredients, is growing (Van Thielen et al., 2018). Under this products and other important quality attributes, such as texture scenario, it is necessary to review the main technologies used. and color. The manufacturing processes start with the post-harvesting of raw insects and ends with the production of foodstuffs and wastes, Drying some of which are recovered and reused as by-products (Raheem Drying is the most widely used technology for increasing the et al., 2018). Although the number of existing processes in the shelf-life of foods. Drying techniques range from traditional meth- edible food industry is enormous and varies depending on the ods (for example, roasting, frying, and sun-drying) to modern species used and the final product to be developed, most of them methods (for example, freeze-drying, microwave-assisted drying), can be grouped into a relatively small number of operations with as shown in Table 4. Drying can reduce the total water content and, the same basic principles, focusing essentially on similar purposes therefore, its availability for degradative reactions, including enzy- (Earle, 1983). These are listed below. matic reactions and reactions initiated by spoilage microorganisms. Microbial growth depends directly on water activity (aw). The vast Blanching majority of microorganisms stop growing at aw <0.65. When aw Blanching is a process wherein a food is placed in boiling wa- is low, microorganisms show slowed growth, and when water con- ter for a short period, removed, and then plunged into ice water ditions are appropriate, they can start growing again (Grabowski or placed under cold running water to stop the thermal process & Klein, 2016, 2017). A reduction of free water increases the dry (Xiao, Bai, Sun, & Gao, 2014). It is used as a pretreatment for most matter concentration significantly without damaging the tissues or commercialized edible insects, at both the industrial and artisanal the physical appearance of foods and is an important step for food scales, to reduce microbial counts and to inactivate degradative ingredient extraction (Lamidi, Jiang, Pathare, Wang, & Roskilly, enzymes responsible for food spoilage and poisoning. As shown in 2019).

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Table 3–Drying treatments used for edible insects.

Edible insect Common name Drying method Conditions used Reference Ruspolia nitidula Grasshopper Air convention dryer. 80 °C/10 hr until moisture of Ssepuuya et al., 2017 5% is reached. Rhynchophorus Palm weevil Solar drying 5 days Tiencheu et al., 2013 phoenicis Oven-drying 50 °C/48 hr Smoke-drying Exposure to smoke heat for 6hr. Sternocera orissa Giant jewel beetle Oven-drying 66 °C/24 hr Shadung, Mphosi, & Freeze-drying −55 °C/24 hr/085 mtorr Mashela, 2012 Frying pan 130-cm diameter, 50-mL tap water Fried without cooking oil Imbrasia epimethea African moth Oven-drying 8 hr/80 °C Lautenschlager¨ et al., Solar drying 3 days 2017 Macrotermes Winged termite Solar drying Approximately 30 °C Kinyuru et al., 2015 subhylanus RH 40% Time not indicated Polyrhachis vicina Black ant Solar drying (20–35 °C until dried, Li et al., 2009 Roger between 2 and 5 days) Ruspolia differens Longhorn grasshopper Freeze-drying Phase (1) −50 °C/0.40 bars Fombong et al., 2017 /48 hr Phase (2) −55 °C/0.021 bars /48 hr Oven-drying 60 °C/24 hr T. molitor Microwave-assisted 8, 10, 13, 16, 20 min Vandeweyer et al., drying 2kw 2017 T. molitor Yellow mealworm Oven-drying Conventional hot air drying Purschke et al., 2018a 60 °C/24 hr 80 °C/7 hr Freeze-drying 0.2 mbars/48 hr Fluidized bed drying Bed temperature: 60 °C Air outlet temperature: 55 °C Differential pressure bed: 15 bar Differential pressure filter: −1.3 bar Air flow: 500 m3/hr Oven-drying with air 45 °C/48 hr Viera-Alves, Sanjinez- circulation Argandona,˜ Linzmeier, Cardoso, & Macedo, 2016 Freeze-drying Not indicated Bußler et al., 2016 Freeze-drying Not indicated Wynants et al., 2018 Cirina forda Moth Oven-drying 40 °C / 24 hr after boiling Omotoso, 2006 Westwood 2hr Rhynchophorus Palm weevil Oven-drying 60 °C to constant weight Idolo, 2010 phoenicis F. Clanis bilineata Dou-Dan Ultrasound-assisted BILON-650CT multi-purpose Sun et al., 2018 aqueous extraction constant-temperature (UAAE) ultrasonic extraction system equipped with one powerful ultrasonic transducer (20 kHz, 650 W)

Sun-drying, freeze-drying, and oven-drying are the preferred crobial contamination and even reduces or removes some harm- technologies for drying whole edible insects, while freeze-drying, ful compounds, such as neurotoxins; it also improves the total oven-drying, and nonconventional drying techniques are used pri- nutritional quality of the product by inactivating protease in- marily for insect flours and powders. Drying and grinding whole, hibitors (Niassy et al., 2016). However, the main limitation of perfectly recognizable edible insects into unrecognizable powders sun-drying is the poor sanitary quality of both the process and the is one of the preferred technologies for increasing human con- final product. The insect is considered dehydrated on the basis of sumption of insects, mostly in the Western countries (Menozzi appearance alone. Moisture content and/or water activity are not et al., 2017). Drying also increases product shelf-life during dis- determined, given that it is a household process. Considering the tribution and storage. However, regardless of the blanching and limited hygiene practices applied during the process, the dried drying treatments applied to insects, they should be reheated be- insects could become contaminated via contact with soil and air fore consumption to eliminate residual microorganisms. Boiling (Caparros Megido et al., 2018). dried insects for 30 min has been found to be a good approach for Smoking is a curing and thermal process. It is considered one eliminating total bacteria, Enterobacteriaceae, Staphylococcus, Bacilli, of the most traditional techniques used for the preservation of all yeasts, and molds (Graboswki & Klein, 2016). types of meat. The raw product is exposed to smoke produced The most traditional drying technology is sun-drying, which by pyrolysis of wood. For insects, smoking is done in a dry en- is used mostly at the household level because of the low en- vironment and a curing process is performed simultaneously with ergy input (required to make products lighter for transportation; drying. During the process, the combined action of enzymes and Azzollini et al., 2016). Sun-drying apparently prevents some mi- heat promotes protein and lipid changes (Tiencheu et al., 2013).

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Table 4–New processing technologies used to extract different compounds of interest from edible insects.

Processing Edible insect technology Purpose Conditions used Reference Tenebrio molitor L. Cold atmospheric Microbiological Surface dielectric-barrier Bußler et al., 2016. pressure plasma charge reduction air-discharge; sinusoidal voltage: 8.9 kVpp; frequency: 3.0 kHz using air as working air with 12 mm of distance below the plasma source; continuous agitation. 350 rpm, 15 min. Thermal load <67 °C. Pimelia spp. Chemical extraction Chitin extraction Dried powder decolorization (6% Kaya et al., 2016 NaClO, 40 °C, 10 min) and demineralization (1% HCl, 35 °C, 2 hr) and deproteinization (NaOH 1M, 70 °C, 10 hr). Wash until pH 7.0 and dried. Holotrichia parallela Chemical extraction Chitin extraction Dried powder milled and treated with Liu et al., 2012 Motschulsky 1M HCl, 100 °C, 30 min to remove minerals and catechol; deproteinization: 1 M NaOH, 80 °C, 24 hr. Washed until pH 7.0. Decolorized (KMnO4 (1%), 1 hr). S. gregaria and A. Sonication assisted Protein extraction Sonication (microtip probe Q Mishyna et al., 2018 mellifera (larvae extraction SONICA); Amplitude: 70; pulse on and pupae) time: 30 s; pulse-off time: 30 s: process time: 6 min; Centrifugation (3,000 × g,20min,4°C). Acidification at pI (4–5) and centrifugation (15,000 × g,20 min, 4 °C); Neutralization (pH 7). S. gregaria And A. Alkaline extraction Protein extraction Dispersion on distilled water (1/15; Mishyna et al., 2018 mellifera (larvae followed by acid v/v); pH = 10 (0.1N NaOH) and and pupae) precipitation stirring 1 hr at 40 °C, Centrifugation (3,000 × g,20min 4 °C). Acidification at pI (4–5) and centrifugation (15,000 × g,20 min, 4 °C). Neutralization (pH 7). S. gregaria and A. Defatting Protein extraction Dispersion on hexane (1/5, w/v) and Mishyna et al., 2018 mellifera (larvae stirring 1 hr and pupae) Re-extraction until clarity and air-drying (35 °C) overnight. Tenebrio molitor L. Supercritical CO2 Oil extraction 400/250 bar, 45 °C, and 105 min. Purschke et al., 2017 extraction Tenebrio molitor L. Dry-fractionation Protein extraction Blanching 10 min 1/12 (w/w) and Purschke et al., 2018a shock-freezing (−38 °C, 20 min); thawing 1 hr, room temperature and drying treatments (see Table 3). Roller milling and sieve classification (pore size 355, 500, 710, 1000, 1400 μm). Locusta migratoria L. Enzymatic hydrolisis Bioactive peptides Hydrolysis conditions (50 °C, pH 8.0, Purschke et al., 2018b production enzyme substrate ratio: 0.05, 0.5 and 1.0 mL/100 mL); Single treatments with alcalase, Flavourzyme, neutrase, and papain or combined treatment: one-step (simultaneously added) or two steps (after 1 hr each); dispersion in water 5% (w/v) (11,000 rpm, 60 s and stirring 1 hr, 50 °C); pH 8.0 addition of enzymes (24 hr, 50 °C). Reaction stopped (90 °C, 20 min). Clanis bilineata Ultrasound assisted Oil extraction Freeze-drying and mixing with Sun et al., 2018 extraction demineralized water (1/6; w/v), blending 5 min. Ultrasound (BILON-650CT multi-purpose); constant- temperature ultrasonic extraction system with 20X; Ultrasonic transducer: 20 kHz, 650 W; Treatment: 400 W, 40 °C, 50 min, and 2 s. Boiled 15 min and centrifugation (12,000 × g,30min,4°C). (Continued)

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Table 4–Continued.

Processing Edible insect technology Purpose Conditions used Reference Tenebrio molitor, Soxhlet extraction Fat extraction Soxhlet apparatus (6 hr, with Tzompa-Sosa et al., Alphitobius petroleum ether as solvent); 2014 diaperinus, Acheta evaporation with rotary evaporator domesticus and at 350 mbar, 40 °C, 30 min. Blaptica dubia, Tenebrio molitor, Water extraction Fat extraction Frozen insect mixed with water and Tzompa-Sosa et al., Alphitobius blended 1 min, followed by 15 min 2014 diaperinus, Acheta of sonication; sieving (350 μm); domesticus and centrifugation 15,000 × g,30min, Blaptica dubia, 4 °C; after separation lipid fraction was centrifuged (15,000 × g,15 min, 40 °C). Tenebrio molitor, Folch extraction Fat extraction Mixed ground powder with 200 mL Tzompa-Sosa et al., Alphitobius dichloromethane/methanol (2:1) 2014 diaperinus, Acheta solution; shaking 20 s; sonication domesticus and 10 min; shaking 2 hr; addition of Blaptica dubia 25 ml of water; centrifugation (1,006 × g,20°C, 20 min). Lipid fraction solubilized in organic solvents and filtered with dichloromethane. Evaporation of solvents 1.5 hr with rotary evaporator (800 mbar). Flushing with N2 in water bath at 40 °C.

Freeze-drying is the most widely used technique for laboratory drying, microwave-drying, vacuum-drying in a vacuum-oven, and analysis of the nutritional characteristics of insects. Given the low conventional-hot-drying on a rotating rack. The authors con- temperature used and the resulting water sublimation, microbio- cluded that all the drying techniques caused minor changes in logical and oxidative degradation ceases to a large extent, thereby protein, fat, and fiber contents. yielding a high-quality final product with excellent nutritional During drying, the most visible quality change relates to color. value and a long shelf-life that is perfect for research but costly to When T. molitor L. larvae powder was oven-dried, color changes scale-up to the industrial level. However, in products with high fat were observed, mostly when compared with fresh freeze-dried content, lipid oxidation could be promoted, as seen in T.molitor L., powders. Lightness values decreased with the blanching and dry- with an attendant decrease in protein solubility (Caparros Megido ing treatments in comparison with fresh freeze-dried samples, as et al., 2017; Kroncke,¨ Boschen,¨ Woyzichovski, Demtroder,¨ & did yellowness (b∗). Redness (a∗) showed no significant changes. Benning, 2018). Freeze-dried edible insects are commonly sold in Oven-drying at 50 °C, followed by a blanching treatment, pre- Europe. Since most studies focus on physicochemical character- served the color in an economical way compared with lyophiliza- ization and provide few or no details on the specific conditions tion (Azzollini et al., 2016). The presence of brown products in applied, it is difficult to compare the results obtained, even for the which acylgylcerides were partially hydrolyzed, accompanied by same species (Caparros Megido et al., 2017). an enrichment of the free amino acid pool, was observed in re- Oven-dried products are comparable to freeze-dried ones, but sponse to a high temperature and short treatment time (90 °C, they have lower energy input costs, reduced lipid oxidation, and 1.5 hr); however, these products had no significant impact on high protein solubility (Fombong et al., 2017; Kroncke¨ et al., chemical composition (Melis et al., 2018). Furthermore, a dark 2018; Lautenschlager¨ et al., 2017). When T. molitor larvae were color appearance was noted after microwave-assisted drying, and dried after blanching in a forced-air oven to moisture equilibrium, the products were considered over processed (Vandeweyer et al., the Page model showed the best fit with an r2 > 0.9932 and the 2017). process presented a type II sorption isotherm (Azzollini et al., The lipid oxidation produced by the different drying processes 2016). negatively affects lipid quality and even the quantity (availabil- Microwave-assisted drying reduced water activity after 16 min ity) of fats present in insects (Qiu, Chen, & Lin, 2019). In the (aw < 0.30), leading to a significant decrease in the microbiolog- case of I. epimethea, the monounsaturated fatty acid content was ical count. The suitability of microwave drying has been tested in slightly reduced when oven-drying was used (Lautenschlager¨ et al., T. molitor L. and final products with an aw below 0.6 were ob- 2017). During smoking, changes in both protein and lipids may tained. Fresh and blanched larvae were dried with minor changes occur. Smoke-drying was performed on Rhynchophorus phoenicis in protein, fat, and ash contents observed in the larvae. More- with the insects spread on a rack. They were exposed to smoke over, the browning index remained constant during 4 months of heat for 6 hr in a traditional way using wood and soot, as this was storage, and the only significant loss relative to freeze-drying con- found to be the best method for maintaining the stability of the sisted of vitamin B12 (Lenaerts, Van Der Borght, Callens, & Van insects’ lipid content (Tiencheu et al., 2013). In T.molitor L. freeze- Campenhout, 2018). However, more studies need to be carried drying oxidized the lipid fraction when compared with other dry- out on how to maintain the sensory quality of the insects when ing techniques such as rack-oven-drying and microwave-drying microwave drying is used (Vandeweyer et al., 2017). with a 4-hydroxy-2-nonenal concentration of 111.03 μg/mL Kroncke¨ et al. (2018) compared various drying processes with (Kroncke¨ et al., 2018). Sun-drying caused an increase in the per- the aim of achieving a moisture content below 7.0% and water ac- oxide value of Rhynchophorus phoenicis, especially if the larvae were tivity under 0.6 in T.molitor L. larvae: freeze-drying, fluidized-bed- previously boiled, probably due to the low water content achieved

r 12 ComprehensiveReviewsinFoodScienceandFoodSafety Vol.00,2019 C 2019 Institute of Food Technologists® Edible insects processing . . . at high temperature during this process (Tiencheu et al., 2013). alyzed. Results showed that pretreatment significantly affects the Organic compounds can also be modified. Following sun-drying color, dimension, density, and other characteristics of the final of Polyrhachis vicina Roger, an edible black ant, aldehydes appeared, dried powders. The sieving fractions had differing macronutrient free fatty acids increased, ketone levels decreased, and hydrocar- compositions and the protein recovery yield was affected as well. bons were found in small concentrations (Li, Sihamala, Bhulaidok, The highest protein recovery was obtained with the particle size & Shen, 2009). Dehydration affects the lipid fraction of edible in- fraction 500 to 1000 μm. Fractionation is, therefore, a promis- sects by decreasing the level of triglyceride unsaturation (Tiencheu ing strategy for producing standardized insect-based intermediates et al., 2013). with a view to industrial applications and consumer acceptance Protein solubility increased in T. molitor L. with vacuum- (Purschke et al., 2018a). drying but it decreased with microwave-drying due to struc- Mishyna, Martinez, Chen, and Benjamin (2018) compared the tural changes that microwaves generated in the protein fraction use of defatting, alkaline extraction, and sonication extraction to (Kroncke¨ et al., 2018). Recently, Huang et al. (2018) compared obtain a protein-rich powder from adult grasshoppers (Schisto- the use of microwave-drying and oven-drying for processing black cerca gregaria) and from honey bee (A. mellifera) larvae and pupae. soldier fly (Hermetica illucens L.) larvae and found that although pro- The three methods were found to be efficient for protein enrich- tein content and quality were similar (showing 40% essential amino ment of the starting materials (powder) from both insects, giving acids), digestibility was significantly higher (greater than 75%) fol- a well-balanced composition of essential and nonessential amino lowing oven drying compared with other drying technologies, acids. For both insects, the highest extraction rate was obtained The application of different drying technologies affects some with defatted raw powder (93.2% and 86.2%, respectively). How- quality parameters beyond the obvious reduction in water. Protein ever, the highest protein extraction rate was obtained with the functional properties, lipid oxidation, and color could be modi- sonication method (57.5 and 55.2 g/100 g dry weight, respec- fied by the drying technology chosen and by the technological tively). Both insect powders showed high foaming and emulsify- conditions applied. Therefore, the choice of drying technology ing capacities that were comparable to whey protein. The highest should take in account the intended use of the insect and the form values were obtained after 120 min for grasshopper powder ex- in which it will be consumed (whole, powdered ingredient, or tracted with sonication. However, changes in protein functionality sole ingredient). Sun-drying should not be considered a primary were found to be related to alteration of protein charge, surface technology, given the associated high levels of lipid oxidation and hydrophobicity, and distribution of proteins. In the case of the poor hygienic conditions. The preferred industrial drying method honey bee, high-molecular-weight proteins (75 to 200 kDa) were is oven-drying since it produces the same final quality as freeze- found, while in the grasshopper, the molecular weight of most drying in terms of protein, fat, and chitin extraction (Azzollini proteins was <100 kDa. The extraction method modified the et al., 2016; Purschke et al., 2018a). molecular characteristics of the proteins, such as surface charge and hydrophobicity. Processing technologies for extraction Enzymatic hydrolysis has been studied mainly with a view New processing technologies for edible insects have been used to gaining a better understanding of the bioactivity of edi- mainly for protein, fat, and chitin extraction as shown in Table 5. ble insects’ hydrolysates after simulated gastrointestinal digestion Protein extraction can be carried out using water, organic sol- (Nongonierma & FitzGerald, 2017), in particular angiotensin- vents, and enzymes to facilitate industrial processes. The extrac- converting enzyme inhibition (Dai, Ma, Luo, & Yin, 2013; Stal- tion rate and characteristics are species dependent and could influ- janssens et al., 2011), and antioxidant capacities (Zielinska´ et al., ence the extraction yield and the physicochemical, functional, and 2017). Changes in the techno-functional properties of enzymatic bioactive properties, depending on the solvent used (Bußler et al., hydrolysates have been explored to a lesser extent, albeit with in- 2016). In T. molitor and H. illucens, an aqueous extraction was used teresting results. In the case of locust Locusta migratoria L. (Purschke to prepare protein-rich intermediates for use in the production of et al., 2018a), techno-functionality was improved by using vari- feed ingredients. To isolate proteins from the insect flours, pro- ous food-grade proteases (alcalase, neutrase, Flavourzyme, papain) tein solubility was optimized by varying the pH, ionic strength, alone or in combination with different enzyme-substrate ratios and extraction temperature of the solvent, and water extraction and hydrolysis times. The solubility, emulsifying, foamability, and was then performed (Bußler et al., 2016). The protein extrac- oil absorption capacities were measured for all the treatments used tion yield in Acheta domesticus was compared using hexane and (higher values were obtained for those with combined enzymes, water in different ratios. Results showed that hexane extraction sequential hydrolysis). This research showed the considerable po- was more effective for yield, color, crude protein, crude ash, and tential offered by targeted enzymatic hydrolysis of edible insects. available carbohydrates. However, water extraction showed better Ultrasound-assisted aqueous extraction was used to extract oil emulsion and foaming capacity, as well as emulsion and foam sta- from Clanis bilineata, an edible Lepidoptera species consumed in bility (Ndiritu et al., 2017). Protein hydrolysates obtained from China, and compared with Soxhlet extraction (Sun et al., 2018). Gryllodes sigillatus crickets using alcalase improved emulsion and The highest oil yield (19.47%) was obtained with the ultrasound foaming properties. The increase in protein solubility also made technique at 400 W ultrasonic power, 40 °C extraction temper- the cricket protein extracts suitable for foods with a pH range of ature, and 2 s intervals for 50 min of extraction. In addition, 3 to 7 and even alkaline conditions (up to pH 10.0) (Hall, Jones, ultrasound extraction improved the amount of polyunsaturated O’Haire, & Liceaga, 2017). fatty acids extracted (56.89 g/100 g of oil) slightly, as well as the Dry fractionation was used successfully with T. molitor L. to ω´ -3/ω´ -6 ratio (4.58). Antioxidant activity was also improved. Ul- increase the yield of protein-enriched fractions, but results were trasound extraction is considered a green technology that provides dependent on the pretreatments and the drying treatment used be- high returns on capital investment as a result of the reduction in fore fractionation (Purschke et al., 2018a). The physicochemical processing time and the quantity of solvents used (Panja, 2018). characteristics of different fractions of T. molitor L. larvae depend Cold atmospheric pressure plasma was applied to T. molitor L. on the drying pretreatment chosen and the sieving fraction an- flour as an innovative pretreatment and compared with thermal

r C 2019 Institute of Food Technologists® Vol.00,2019 ComprehensiveReviewsinFoodScienceandFoodSafety 13 Edible insects processing . . .

Table 5–Edible insect commercial brands/companies and their marketed products.

Brand/Company Products Country Source Aldento Pasta with Tenebrio molitor. Belgium https://www.goffardsisters.com Aketta Roasted cricket and powder. USA http://www.aketta.com/ Bitty Foods All-purpose cricket flour. USA Sold on Amazon US Chapul Cricket energy bars and protein USA https://chapul.com powders Chirps/Six Foods Cricket chips USA Sold on Amazon US Cricket Flours Crickets and mealworm powder and USA https://www.cricketflours.com whole cooked insects Exoprotein Energy and protein bars with cricket USA https://exoprotein.com/ protein and roasted, flavored crickets Griopro Cricket powder USA https://cricketpowder.com Hotlix Candies, lollipops and flavored USA https://hotlix.com crickets, scorpions, and larvae. Entovida Wide range of edible insect cooked USA https://www.entovida.com ready-to-eat products: maguey worms, bamboo worms, scarab beetles, silkworms, ants, chapulines (grasshoppers), hornets, wasps and bees, crickets, mealworms, waterbugs, and scorpions. Meat Maniac Seasoned and flavored crickets, USA https://www.meatmaniac.com termites, scorpions, mealworms, water bugs, rhino beetles, centipedes, cicadas, earthworms, shield bugs, zebra tarantulas, and locusts. Newport Jerky Cricket powder, canned scorpions, USA http://www.newportjerkycompany.com Company worm suckers, and mixed pupae. All Things Bugs Premium cricket powder (finely USA http://allthingsbugs.com/ milled). Bud’s Cricket Cricket protein powder USA https://budscricketpower.com Power Bugeater Foods Bugs-a-Roni (Pasta), Jump Taste USA https://www.bugeaterfoods.com/ (protein cricket powder). Critter Bitters Cocktail bitters made with toasted USA http://www.critter-bitters.com/ crickets. Cricket Flours Roasted cricket bites, cricket flours USA https://www.cricketflours.com/ brownie mix, buffalo wing sauce cricket bites, cricket flours: pure powder, cricket salt (3 flavors). LANDISH Cricket powder superfood bars, USA https://landish.co/ Superfood protein powder (cricket powder), crickstart crackers. Detroit Ento Cricket powder USA https://www.detroitento.com/ Don Bugito, Chile-lime crickets with pumpkin USA https://www.donbugito.com/ Prehispanic seeds, dark Chocolate covered Snackeria crickets, spicy bugitos (worms), coconut toffee-brittle bugitos, cricket protein powder, granola bites powered by cricket flour, chinicuil (worm) salt. Entosense Edible insect marketplace (from ants USA https://www.entosense.com/ to zebra tarantulas). Jurassic Snacks Powdered peanut butter enhanced USA http://www.jurassicsnacks.com/ with cricket powder, cricket power powder. Lithic Cricket protein powders, cricket USA https://www.lithicfoods.com/#Products protein bars, cricket pasta, pure cricket flour, all-purpose cricket flour, and cricket protein snack bars, among others. Seek-Food Cricket protein powders, gluten-free USA https://seek-food.com/ cricket flour, and paleo cricket flour. Crunchy critters Chocolate covered, powder, and United Kingdom https://www.crunchycritters.com tubes of crickets, larvae, mealworms, buffalo worm, and locust. Eat Grub Energy bars, powders, roasted United Kingdom https://www.eatgrub.co.uk/ flavored crickets, buffalo worms, and mealworms. Kric8 Cricket protein powder and pasta. United Kingdom https://www.kric8.co.uk/ MiniFeasts British dried-farmed mealworms United Kingdom https://www.minifeasts.co.uk/ (original, rosemary & salt, chili and lime, chili and red pepper) and insect flour. NutriBug Cricket powder (75% protein), United Kingdom https://nutribug.com/ cricket powder (76% protein), cricket protein bars, and cricket protein pasta. r (Continued) 14 ComprehensiveReviewsinFoodScienceandFoodSafety Vol.00,2019 C 2019 Institute of Food Technologists® Edible insects processing . . .

Table 5–Continued.

Brand/Company Products Country Source Yumpa Energy bars made with United Kingdom http://www.yumpabar.co.uk/ protein-packed cricket flour. Zoic Bar High protein insect bars (cacao and United Kingdom Facebook https://www.facebook.com/zoicbar/ tarragon). Delibugs Freeze dried, energy bars, candy & Netherlands https://delibugs.nl/ lollipops, spreads, made from a wide variety of insects. Burgs Foods The Dutch bugburger. Netherlands http://www.burgsfoods.nl/ De Krekerij Variety of products including Netherlands https://krekerij.nl/ crickets and grasshoppers, cricket meat, and catering service based on insect-based products. Kreca Ento-Food Buffalo insect powder, freeze-dried Netherlands https://www.krecafood.com/ BV crickets, whole insects (freeze-dried buffalo worms, grasshoppers, mealworms), insect powder (cricket, mealworm, grasshoppers). Tiny Foods Freeze-dried insects, seasoned Netherlands https://tinyfoods.nl/ insects (buffalo worms, house crickets, mealworms, grasshoppers), protein bars and energy bars, sweets and snacks, house crickets, mealworms, and so on. Tjirp Insect Food Insect-based croquette snack. Netherlands https://www.tjirpfood.nl/ Europe- Dried insects, insect candy, and France http://www.europe-entomophagie.com entomophagie wholesale mealworms, scorpions, crickets, silkworm, caterpillars, ants, termites, and giant worms in kilo packs. ¨Ihou The houtou products are sourced France http://ihou.fr/ exclusively from their farming operation based in eastern France. Dehydrated crickets (salted, sweet, chili, and natural). Insect´eo Black scorpions, mix of insects to France https://www.insectescomestibles.fr/ discover, natural crickets, vodka brewed with different types of insects (scorpion, termites, chenille), curry, flavored roasted, flour, lollipops, pat´e, and cricket energy bars. Insect´eo Flavored and seasoned crickets, France http://www.insecteo.com mealworms, and scorpions. GRYO¨ Insect health food snacks (cricket France http://gryo-food.com/#!home/mainPage powder bars). Jimini’s Spiced, Greek spice, fruity curry and France https://www.jiminis.com/ paprika snack insects and high protein bars, insect flours for sport nutrition, high protein insect pasta, and so on. Micronutris Insect crackers (chili, thyme, sesame, France https://www.micronutris.com/fr/accueil tex-mex), cooking packs with dehydrated insects, high protein bars, including mealworm bars. MinusFarm Biscuits made from mealworms and France https://minusfarm.fr/ crickets, Macarons made from mealworms and almonds, and so on. Mon grillon Cricket protein bar, High protein France/UK https://www.inpulseprotein.com/ (Inpulse cricket powder. protein) future foods Bug Biters Chocolates with grasshoppers, Mexico On Facebook Corporation cricket tortillas, cricket protein (www.facebook.com/Bug-Biters-1628 banana pancakes, cricket protein 02594219573/) powder,andsoon. Gran Mitla Agave worm salt 100% chinicuil, Mexico https://granmitla.us/ grasshopper salt, ground agave worms. Griyum Cricket protein powder (60% Mexico https://www.griyum.com.mx/ protein), and local cricket farms. Merci Mercado Gourmet seasoned chapulines Mexico http://mercimercado.com (grasshoppers), agave worm salt, red maguey worms, and ground grasshoppers. (Continued)

r C 2019 Institute of Food Technologists® Vol.00,2019 ComprehensiveReviewsinFoodScienceandFoodSafety 15 Edible insects processing . . .

Table 5–Continued.

Brand/Company Products Country Source Snack insects Roasted, chocolate covered, energy Germany https://wuestengarnele.de bars, candy & lollipops, and spreads of mealworms, and crickets. BugFoundation Germany’s first insect burger made Germany https://bugfoundation.com/home-en. from buffalo worms. html BenetoFoods BenetoFoods is a new innovative Germany https://www.benetofoods.com/ food company that produces high-protein and high-quality foods based on barbequed protein. Three different flavors of cricket pasta. Brento Delicious breads (Paleo-brento, Germany https://brento.de/ Urkorn-brento, Ciabrento) with buffalo insect flour. Instinct (Insek- Organic insect snacks (bars, apple Germany https://www.yourinstinct.de/ tensnack) and cinnamon, salty chocolate). Isaac Nutrition Insect flour (cooking and baking), Germany https://isaac-nutrition.de/ protein powder with insects. Imago-Insects Cricket Burger Quinoa, Cricket Germany https://www.imago-insects.com/ Falafel Curry, Cricket Bolognese, Cricket Burger Classic, crispbread with flaxseed, and so on. Plumento Foods Products such as pasta, biscuits, Germany https://plumento-foods.com/ granola and croutons. These are high-quality, tasty products in which insects are disguised constituents. Snack-Insects Snack-Insects offers fine Germany https://snackinsects.com/ grasshoppers, crickets, and flour, buffalo worms from selected European breeders. Insect-based foods such as power bars, insect pasta and granola. Swarm Protein Snack high protein bars. Germany https://swarmprotein.com/ Wicked Cricket Insect power bars, insect snacks, Germany https://wickedcricket.de/ crickets as snacks (salt, pepper and herbs). Vitabug Flavored roasted, chocolate covered, Australia https://ediblebugshop.com.au/ tortilla chips, and marshmallows of crickets, mealworms, and ants. Bugsy Bros Crispy baked crickets, 100% cricket Australia http://bugsybros.com.au/ powder, protein ball mix, sample packs, among others. The Cricket Effect Protein packed muesli bars with Australia https://thecricketeffect.weebly.com/ cricket flour. The Cricket Insect-based baking blends (banana Australia https://thecricketbakery.com/ Bakery bread, protein pancakes, protein powder, and seedy paleo loaf). Grilo Protein Organic cricket protein powder, Australia https://griloprotein.com.au/ organic super greens & cricket, organic roasted crickets, organic cricket energy bar (different flavors). GrubsUp Whole roasted crickets, whole Australia https://grubsup.com.au/ roasted mealworms, cricket energy bar, cricket hazelnut dukkha, and cricket powder. Leap Protein Peanut Butter Cricket Protein Bar, Australia https://www.leapcricketproteinbars.com/ Cricket Skin Glow Bar (Orange & Goji Berri), Cricket Protein Bar (Chocolate Coconut). Primal Collective Roasted crickets. Australia https://www.optimoz.com.au/products/ roasted-crickets-edible-bug-protein Hopper Foods Flavored granola bars with cricket Australia https://hopperfoods.com.au/ flour Die Wurmfarm Worm Gourmet Gastronomy Austria https://www.diewurmfarm.at/gastronomie/ (mealworm based products). Insekten Essen, Mealworms, buffalo worms, locusts, Austria https://www.zirpinsects.com/ Zirp Insects crickets, Sauces (pesto and basil, tomato pesto with buffalo worms), bug snack, Zirp Zotter (dark chocolate 70% and dark chocolate 80% and Zirp Buffalo Worms) Beesect: Beetles A unique beer, flavored with protein Belgium http://www.beetlesbeer.be/en/ Beer from insects. Bugs World The LIZZY bitterballen; A healthy Belgium http://www.bugsworldsolutionfood.com/#3 Solution Food variant of the typical “meat bitterball,” insect snacks, etc. (Continued) r 16 ComprehensiveReviewsinFoodScienceandFoodSafety Vol.00,2019 C 2019 Institute of Food Technologists® Edible insects processing . . .

Table 5–Continued.

Brand/Company Products Country Source Goffard Sisters Artisanal pasta (enriched with Belgium http://www.goffardsisters.com/ mealworms). Kriket KRIKET is a delicious snack made Belgium https://kriket.be/ from a mixture of nuts, grains, seeds and crickets, and 100% sourced in Brussels. Little food Powder, tapenade, crickers (Cricket Belgium https://www.littlefood.org/ Crackers) and dried crickets. Nimavert Ravioli and croquettes with Belgium https://www.nimavert.be/nl mealworms as a main ingredient. Bite Snacks Energy bars and cricket protein Canada https://bitesnacks.com/ powders. C-FU Foods Extracts the protein from crickets Canada https://cfufoods.com/ and makes their own cricket-tofu: C-FU. CrikNutrition Protein powders (crickets, chocolate, Canada https://criknutrition.com/ sweet vanilla, etc.). Coast Protein Protein energy bars, cricket protein Canada https://www.coastprotein.com/ powders. Fit Cricket Cricket protein powder and protein Canada https://fitcricket.com/ Nutrition bars. Inspiro Foods Insect protein products Canada http://www.insprofoods.com/ NAAK¨ Cricket products: energy bars, Canada https://naakbar.com/ energy bits, high protein bars, cricket protein powder. Tottem Nutrition Pasta + cricket powder Canada https://tottemnutrition.co/ uKa prot´eine Cricket flour, roasted crickets. Canada https://ukaproteine.com/ Yes Crickets Crickets (Acheta domesticus). Canada https://www.yescrickets.com/ Premium Canadian cricket farm growing crickets and also selling flavored dry-roasted crickets and protein powder. Entomofarms Cricket powder, mealworm protein Canada https://ca.entomofarms.com powder, seasoned and flavored crickets and mealworms. Bugsolutely Making the Bella pupa silkworm China https://www.bugsolutely.cn/eng/ China snack. BioHexaPro Will produce burgers, protein bars, Colombia https://www.biohexapro.com and cricket flour for Agriculture and Pet Food. (Started January 2018) 1900 Especies Farming, commercialization and Colombia https://1900especies.co/ traditional cooking methods of insects for human consumption. Sensbar Protein bars & energy bars made Czech Republic https://www.sensbar.com/en/ with cricket flour (different flavors). Crickster Cricket protein flour and whole, Denmark https://crickster.dk/ Buffalo worm flour and whole, Snack crickets (different flavors umami, Mexican and Italian). Enorm Danish company making insect bars Denmark http://www.enormfood.com/ with lesser mealworm (and other snacks with chili, onion, and so on). Syngja Cricket shot with different flavored Denmark https://syngja.dk/ drinks (apple ginger, beetroot seaberry, and spirulina acerola). Wholi foods Used to be known under the brand Denmark https://wholifoods.com/ “Dare to eat.” Makes cricket snacks and a protein bar called “Buff bar,” buffalo larva flour, Dare squares (chili, chocolate & cricket), peanut butter and buffalo worms, and so on. Entis BUGBITESR is an insect and Finland https://www.entis.fi/ vegetable protein-based snack, SirkkisR is a tasty protein product containing vegetable proteins and cricket powder, SirkkasuklaaR -chocolate covered crickets. Finsect/GRiiDY Northern forest cricket crackers, Sea Finland http://www.finsect.fi/ salt roasted crickets, Soy and ginger roasted crickets, Garlic salted roasted crickets, and warm chili roasted crickets. Griinsect Griinsect cricket crackers Finland http://www.griinsect.fi/ (seed-cricket-snack). Leader Zircca bar Nutritious and sustainable bars Finland http://www.leader.fi/eng/products/zircca/ made of cricket’s protein. (Continued) r C 2019 Institute of Food Technologists® Vol.00,2019 ComprehensiveReviewsinFoodScienceandFoodSafety 17 Edible insects processing . . .

Table 5–Continued.

Brand/Company Products Country Source Nordic Insect Dried insects. Finland http://nie.fi/ Economy Savonia Grasshopper (hot pepper, Finland https://sirkkoja.fi/ Grasshopper herb-garlic, sweet), Roasted hopper, Grasshopper chips. Biteback Using edible insects (meal worm oil) Indonesia http://www.bitebackinsect.com/ as a healthier and more sustainable source of fats and oils. Crick´e Cricket crackers and cricket powder. Italy https://crickefood.com/ Italbugs Italian food (pasta) and sport Italy http://www.italbugs.com/ supplements (protein powder and bar) from insects. Insetti A wide variety of products: Mix of Italy http://www.insetticommestibili.it/ commestibili insects (dehydrated), cricket flour, insect protein bars, silk worm flour, canned insects, and so on. The flying spark Working with fruit fly larvae. The Israel https://www.theflyingspark.com/ currently produce whole high-quality protein powder, reduced-fat powder, dry larva, and larvae oil. Bugmo Cricket bars and cricket flour. Japan https://bugmo.jp/ Eat Crawlers Salted caramel scorpions, Lightly New Zealand https://www.eatcrawlers.co.nz/ salted insect mixture, Zebra tarantula (dehydrated), freeze-dried crickets and scorpions. Live Longer Cricket flour (100% organic), cricket New Zealand https://livelonger.co.nz/ protein bars. Primal future Premium Organic Cricket Powder. New Zealand http://www.primalfuture.co.nz/ Acheta Cricket powder. Norway https://acheta.no/ Invertapro High-quality protein and plant Norway https://www.invertapro.com/ nutrition based on the Tenebrio molitor larvae (Mealworm) and Hermetia illucens larvae (Black soldier fly). UNIKMAT Insect flour, insect protein bars, Norway https://www.unikmat.no/ whole billbill larvae, Siris flour (100% Acheta siris). Urbanmat Breeding and selling insects both Norway https://www.urbanmat.no/ whole and prepared. Mopani Queens The only company in South Africa South Africa Mopani Queens Facebook page. and sells flavored Mopani Caterpillars or Mopani Worms. Barbeque, chili, chutney, and the original salted flavor. Edible-bug Dried edible insects, edible cranberry South Korea https://edible-bug.co/ cookie, and meal worm powder. EntomaFoods Snacks, whole dried insects, insects’ Spain https://entomafoods.com/es/ flours, protein bars, seasoned dried Tenebrio molitor,seasoned grasshoppers, and so on. EAT:EM Cricket bars, Crisp Bread (with Sweden http://www.eatem.se/ crickets), and crackers. /NUTRIENT The first Swedish entrepreneur Sweden https://www.nutrient.se/ breeding its own mealworms. Tebrito Working on their own protein Sweden http://www.tebrito.se/ product based on mealworms. Essento Mealworms burgers and balls. Switzerland https://essento.ch/ Entomos Swiss organic mealworms Tenebrio, Switzerland https://entomos.ch/ house crickets’ acheta,edible grasshoppers (lyophilized), grasshoppers Locusta, protein balls with cricket, pastry with cricket flour, crisps with organic Tenebrio molitor, among others. Insekterei Pat´e with mealworm, crispbread Switzerland https://insekterei.ch/ with cricket flour, high-quality protein cricket balls, and dried crickets’ powder (Protein 60%). Hiso Wide range of cooked and flavored Thailand http://www.hisoapero.com silkworms and crickets. JR Unique Foods, Cricket powder, fried cooked pupae, Thailand https://jrunique.com (sold also and scorpions. under the brand name of EcoEat) (Continued)

r 18 ComprehensiveReviewsinFoodScienceandFoodSafety Vol.00,2019 C 2019 Institute of Food Technologists® Edible insects processing . . .

Table 5–Continued.

Brand/Company Products Country Source Next-food Flavored crickets, Plain roasted Thailand https://www.next-food.net scorpion, tarantulas, mealworms, giant water bug, giant worms, silkworms, locust, grasshoppers, diving beetle, weaver ants, bamboo worms, cicada, and ants. Bugsolutely Cricket pasta, snack with insect Thailand https://www.bugsolutely.com/ powder (silkworms), Bella Pupa. Get propro Cricket protein bars with different Thailand https://www.getpropro.com/ flavors, Thailand Unique Canned, bulk, candies and powders Thailand https://www.thailandunique.com of a wide variety of insects including crickets, dung beetles, larvae, pupae, shield bugs, scorpions, black ants, cicada, weaver ants, silk month pupae, ant eggs, squash bugs, and grasshoppers. (All web pages accessed April 01, 2019). treatments between 20 and 140 °C at different times to reduce Three-dimensional food printing technologies have recently microbiological loads. Although high temperature treatments (120 been used to extrude insect paste filaments as a new method to 140 °C) inactivated all the microbiota present in the insect, the for creating foodstuffs. This is an innovative manufacturing pro- use of cold atmospheric pressure plasma reduced microbiological cess whereby a digitally controlled robotic construction process loads by up to 3 log units, and the overall quality of the final prod- can make three-dimensional objects based on layer-by-layer de- uct was better. The T. molitor L. flour through cold atmospheric position (Severini, Azzollini, Albenzio, & Derossi, 2018; Soares & pressure plasma processing showed better thermo-functional prop- Forkes, 2014). Previously ground microwave-dried T. molitor lar- erties such as water and oil binding capacities and protein solubility vae were used to enrich a wheat dough, and the three-dimensional when extraction was performed at pH 4.0. Some changes in pro- printing process was performed using a three-dimensional printer tein composition were also found as a decrease in low-molecular model equipped with a clay extruder. The dough was pushed by a fractions (15 to 20 kDa) and an increase in high-molecular frac- piston at a pressure of 4 bars through a plastic tube on the head of tions (>60 kDa; Bußler et al., 2016). the extruder. The printing conditions were as follows: print speed Purschke et al. (2017) studied supercritical CO2 extraction of 30 mm/s, travel speed 50 mm/s, layer height 0.5 mm, and nozzle edible insect oil from T.molitor L. larvae. The authors found that T. size 0.84 mm. The printed snacks reproduced the overall structure molitor oil composition and acidity was influenced by the extraction of the designed object, but the addition of different concentra- parameters. Extracted oils contained 72% unsaturated fatty acids, tions of the insect powder modified the printability of the dough and an oleic acid content close to 42% with a high oil extraction and the morphological and microstructural properties of the final yield (95%). Oil composition and acidity were affected by the product. However, the nutritional quality was greater than that of extraction parameters, with better results obtained at low pressures the nonsupplemented wheat dough (Severini et al., 2018). and temperatures. However, the oil composition was similar to that Borremans et al. (2018) carried out marination and fermen- of hexane-extracted oil. tation of T. molitor larvae, a novel culinary practice, and found Tzompa-Sosa, Yi, van Valenberg, van Boekel, and Lakemond that these processes provided final products with a long shelf- (2014) extracted lipids from Tenebrio molitor, Alphitobius diaperinus, life; they did not evaluate consumer acceptance. In the study, Acheta domesticus,andBlaptica dubia using three methods: Soxhlet blanched larvae were marinated for 6 days in either red wine or soy extraction, aqueous extraction, and Folch extraction. T.molitor had sauce. Both treatments were effective in preventing the prolifera- the highest lipid content among the four species, and the highest tion of spoilage microorganisms (total viable aerobic microorgan- extraction yield was obtained with the Folch extraction method. isms, Enterobacteriaceae, and bacterial endospores), and mealworm The method used affected the quantity of lipids obtained as well shelf-life was extended for 7 days relative to larvae that were only as the lipid profile. Water extraction gave the best lipid profile blanched. In the fermentation treatment, larvae were crushed prior quality, even when the extraction yield was the lowest. to fermentation in order to obtain a paste and were inoculated Chitin and chitosan are extracted from the exoskeletons of a with a mixture of Pediococcus acidilactici, Lactobacillus curvatus, and variety of edible insects. This is the case for the beetle Holotrichia Staphylococcus xylosus meat starter, supplemented with 2.8% NaCl parallela Motschulsky that is captured for the control of pests in (w/w), 0.75% d-(+)-glucose (w/w), and 0.051% NaNO2 (w/w), fields. This insect’s chitin was compared with the commercial α- and then incubated at 35 °C for 2 weeks until fermentation was chitin extracted from shrimp. The beetles’ chitin showed similar complete (pH < 5.0). The shelf-life of the two products was not characteristics to the chitin obtained from shrimp. Chitin from H. determined (Borremans et al., 2018). parallela could be an alternative source of chitin (Liu et al., 2012). A similar extraction was performed on exoskeletons of Pimelia spp. Storage The extracted chitin and chitosan were found to be nontoxic and In many parts of the world, “ready-to-eat” insects are sold showed antimicrobial activity against C. albicans and L. monocy- in local markets after sun-drying, roasting, or frying in bulk togenes, and therefore has potential for use in food preservation. without appropriate hygienic handling. When insects have not The oil-binding properties of chitin are well documented and can previously been subjected to a thermal treatment, such as boil- be used to design potential oil-binding food supplements (Kaya, ing, they may contain a high microbiological load and they can Sargin, & Erdonmez, 2016). be recontaminated and/or cross-contaminated. Therefore, it is

r C 2019 Institute of Food Technologists® Vol.00,2019 ComprehensiveReviewsinFoodScienceandFoodSafety 19 Edible insects processing . . . necessary to process, pack, and store them properly to minimize in raw minced meat from traditional sources. The product shelf- the bacterial loads. Since blanching does not eliminate bacterial life also depended on the original minced species used. How- spores (Belluco et al., 2013; Caparros Megido et al., 2018), to ever, the specific presence of food pathogens should be analyzed completely sterilize insect flours, thermal treatment at a temper- before this type of product is stored in modified atmospheres ature between 120 and 140 °Cneedstobeappliedfor15min (Stoops et al., 2017). Similar results were obtained by Flekna, (Bußler et al., 2016). Recontamination and cross-contamination Make,¨ Bauer, and Bauer (2017), who found that under anaerobic can occur when products are improperly packed and stored, even if conditions, T. molitor (30% CO2; 70% N2) can be preserved for 3 a blanching process was performed. In the case of blanched, dried, weeks under refrigeration without microbial changes or oxidative and ground A. domesticus, the flour could be preserved for 16 days deterioration. with refrigeration (5 to 7 °C), but only 4 days at room temperature (28 to 30 °C; Klunder, Wolkers-Rooijackers, Korpela, & Nout, Commercialization of Edible Insects 2012). Edible insects have traditionally been sold dried and/or ground In general, storage conditions depend on the insect species and and are sometimes marketed as flours, heat-dried larvae, pupae, on whether the product is sold as whole and ready-to-eat in- or whole adult insects. Edible insects are available in the market sect or as a powder, after a drying process. Each product type in a variety of forms: canned, bulk, powder or flour products, displays a specific pattern of shelf-life, consisting of the sum of snacks, candies, chocolate-covered, and liquor infusion. Thailand the raw product initial counts, plus modifications due to pro- UniqueTM (JR Unique Food Ltd.), an online retailer, sells a range cessing as well as secondary contamination (Grabowski & Klein, of products, from canned items to more processed forms, such as 2017). pasta and protein shakes. Over the last 10 years, several companies Recently, Adamek´ et al. (2018) analyzed the microbiological and startups around the world, mainly in Europe, South Asia, and quality of the following long-term-stored edible insects: yellow North America, have been created to commercialize insect-based mealworm (Tenebrio molitor), lesser mealworm (Alphitobius diaperi- food products for human consumption. Approximately, 133 of nus), field cricket (Gryllus assimilis), and migratory locust (Locusta these brands/companies are listed in Table 5. On Amazon.com migratoria). All the samples were found to be safe for human con- (USA) alone, more than 100 insect-based food products sumption. The most suitable processing for long-term storage was are sold as gourmet foods (https://www.amazon.com/s?k= killing with boiling water, drying at 103 °C for 12 hr and subse- edible±insects&__mk_es_US=%C3%85M%C3%85%C5%BD% quent hermetic packaging. C3%95%C3%91&ref=nb_sb_noss_2), most of which are sold In the case of fresh insects, freezing (−20 °C) is recommended in whole form. On eBay, over 250 edible insect’ food prod- as a storage method to maintain their microbial quality instead of ucts are available (https://www.ebay.com/sch/i.html?_from= refrigeration (5 to 7 °C; Belluco et al., 2013). For dried and pow- R40&_trksid=m570.l1313&_nkw=edible±insects&_sacat=0). dered edible insects, refrigeration is the best method for avoiding For instance, the French brand Insectes ComestiblesTM oxidative and microbiological degradation. Similar results were (www.insectescomestibles.fr) sells curry, lollipops, pate´ and energy obtained for field crickets (Gryllus bimaculatus) and superworms bars, and other products made from crickets (A. domesticus). (Zophobas atratus) (Grabowski & Klein, 2016). According to our research on insect-based food businesses, the When refrigeration is combined with vacuum or modified at- main commercial forms are flavored snacks, energy bars, and mospheres, the shelf-life of the products increases markedly. Stor- powders (sold mainly as sports supplements) and the most widely age under vacuum and darkness can improve the shelf-life of whole sold insects are crickets, grasshoppers, and mealworms (see edible insects even when stored at room temperature (Ssepuuya, Table 5). Aringo, Mukisa, & Nakimbugwe, 2016). Vacuum packing im- Due to their high levels of proteins and well-balanced amino proves the microbiological quality of the product, while darkness acid profile, insects have attracted the attention of researchers prevents lipid oxidation. For instance, whole Ruspolia nitidula (a as potential food ingredients for sports nutrition supplements, grasshopper), when pan-fried and dried, maintained edible quality such as protein concentrates/isolates, flours, energy bars, protein (sensory and microbiological) for 12 weeks. No significant differ- shakes, and hydrolysates. These products, most of which are made ence in total plate counts was observed when vacuum (reduced with crickets and mealworms, are sold in specialized stores, (see pressure) was applied (Ssepuuya et al., 2016). In addition, vacuum Table 5). T. molitor L. has been used to fortify a wide variety storage can maintain the microbial (total plate count), sensory of foods, such as corn tortillas, cookies, and meat-like products. (overall acceptability), and chemical properties (acid value, per- In corn tortillas, this insect has been used as a supplement (2%, oxide value, and thiobarbituric acid values) of ready-to-eat R. w/w). When corn tortillas supplemented with 7.14% T. molitor nitidula for 22 weeks similarly to low-temperature storage (Ssepu- larvae flour, the supplemented tortillas were 2% higher in pro- uya, Mukisa, & Nakimbugwe, 2017). tein (Aguilar-Miranda, Lopez,´ Escamilla-Santana, & Barba de la A modified atmosphere consisting of 60% CO2 and 40% N2 Rosa, 2002). Freeze-dried T. molitor L. larvae were used to en- was used to store minced meat-like products from T. molitor rich emulsified sausages, resulting in an improvement in emul- and Alphitobuous diaperinus larvae under refrigeration. A signif- sification properties (Kim, Weaver, & Choi, 2017). Cho, Zhao, icant reduction in microbial growth was observed relative to Kim, Kim, and Chung (2018) developed a liquid seasoning fer- samples stored in normal atmospheric conditions. The T. m o l i - mented by Aspergillus oryzae and Bacillus licheniformis for addition tor aerobic count remained low (1.0 log CFU/g) after 28 days to the soy sauce fermentation process, producing sensory prop- when stored under modified atmosphere; however, the total aer- erties similar to those of the original soy sauce; however, 1.5 obic count was 6.9 log CFU/g for samples stored under am- to two times more essential amino acids than the soy-fermented bient conditions. By contrast, A. diaperinus could be stored for sausage. only 14 days under modified atmosphere conditions (1.9 log Minced meat-like products with a mealworm larvae content of CFU/g). Bacterial community composition differed between the more than 90% were successfully produced and stored in modified two stored products but was significantly lower than that found atmosphere packaging for 14 to 28 days, depending on the insect

r 20 ComprehensiveReviewsinFoodScienceandFoodSafety Vol.00,2019 C 2019 Institute of Food Technologists® Edible insects processing . . . species used (Stoops et al., 2017). Meat batters containing 5%, somewhat interested in healthy and ethnic foods. The consump- 10%, and 15% edible silkworm pupae and transglutaminase were tion of whole insects is the main issue that needs to be addressed added to frankfurters, resulting in higher protein and ash contents in the short term, possibly through offerings such as snacks and and significantly lower cooking loss weight than in the control. In energy bars. Some insect-based ingredients have substantial po- addition, the silkworm pupae meat batter showed an increase in tential owing to their nutritional characteristics and functional pH value, viscosity, and texture properties compared to the control properties in food, pharmaceutical, and cosmetic products. For (Park et al., 2017). instance, protein concentrates and/or isolates derived from insects Sun-dried termites were used to formulate an extruded prod- have high foaming and emulsifying properties, as well as other uct (winFoodR ) containing germinated amaranth, white corn, techno-functional capacities. Insects are rich in polyunsaturated soybean oil, and sugar to combat infant malnutrition in Kenya fatty acids and have a high ω´ -3/ω´ -6 ratio. The chitin composition (Kinyuru et al., 2015). Prior to extrusion, the insects were sub- of insects is similar to that of shrimp, making them a feasible and jected to blanching (95 °C, 1 min) and oven drying (120 °C, sustainable option for replacing some currently available functional 1 hr). Extrusion was carried out using a locally fabricated ex- ingredients. These aspects should be a focus of future research and truder with a barrel length/diameter ratio of 25. The extrusion technological development. conditions were as follows: feed moisture content 12% to 14.4%, moisture injection 9%, feed rate 33 kg/hr, screw-speed 300 rpm, and barrel temperatures 70 °C (zone 1), 100 °C (zone 2), and Acknowledgment 127 °C (zone 3). Results showed a low-cost process and a final This research did not receive any specific grants from fund- product with good nutritional value and a shelf-life of 6 months ing agencies in the public, commercial, or not-for-profit sectors. (Kinyuru et al., 2015). The macro-termite Macrotermes subhyalinus The authors wish to express their gratitude to Dr. Martin Mon- was used to design sorghum biscuits. The termites were cleaned dor of Agriculture and Agri-Food Canada, in Saint-Hyacinthe, and oven-dried at 65 °C for 72 hr before blending. The flour was Quebec, Canada, for his comments and support, as well as Chef dispersed in hexane for 1 hr, and the mixture was decanted under Mario Melgarejo Pin˜on´ for kindly providing the pictures for reduced pressure to separate the solvent. The residue was dried at Figure 2. room temperature for 24 hr and preserved at 4 °C. Biscuits were formulated with different concentrations of the protein extracted from the insect. Results showed a significant improvement in the Author Contributions protein and mineral contents of the biscuits. The sensory analysis Melgar-Lalanne and Hernandez-´ Alvarez´ collected most of the showed that the biscuits are acceptable with an insect flour content data, wrote the draft manuscript, and suggested the original idea of up to 25% (Niaba Koffi et al., 2013). for this review. Salinas-Castro collected and reviewed the data for Flour produced from the cockroach Nauphoeta cinerea was used the insect farming section. All of the authors reviewed the entire to enrich bread at concentrations between 5% and 15%. The flour document and approved the final version. presented satisfactory sanitary conditions with a good nutritional profile due to the amino acid and fatty acid contents, and ad- dition of the insect flour did not alter the technical or sensory Conflict of Interest characteristics (de Oliveira, da Silva Lucas, Cadaval, & Mellado, The authors do not have any conflicts of interest to declare. 2017). Crickets have been used to formulate cookies with amaranth, rice, oatmeal, chocolate chips, butter, walnuts, and so on. (Ayieko, References Ogola, & Ayieko, 2016; Ryu, Shin, Kim, & Kim, 2017) and these Adamek,´ M., Mlcek,ˇ J., Adamkov´ a,´ A., Suchankov´ a,´ J., Janal´ıkova,´ M., products are well accepted by children (Ayieko et al., 2016). Borkovcova,´ M., & Bedna´ˇrova,´ M. (2018). 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Characteristics of maize flour tortilla supplemented with vironmental, technological, and nutritional advantages associated ground Tenebrio molitor larvae. Journal of Agricultural and Food Chemistry, 50(1), 192–195. https://doi.org/10.1021/jf010691y with insect agriculture. Alemu,M.H.,Olsen,S.B.,Vedel,S.E.,Pambo,K.O.,&Owino,V.O. (2017). Combining product attributes with recommendation and shopping Conclusions location attributes to assess consumer preferences for insect-based food New food processing technologies are required to formulate products. Food Quality and Preference, 55, 45–57. functional ingredients and snacks in whole and recognizable forms, https://doi.org/10.1016/j.foodqual.2016.08.009 Armelagos, G. J. (2014). Brain evolution, the determinates of food choice, in order to promote entomophagy. The benefits of increasing in- and the omnivore’s dilemma. 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